Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice
PurposeGut microbiota dysbiosis significantly impacts ulcerative colitis (UC) progression and exacerbation. Probiotics show promise in UC management. This study evaluated the effects of different doses of Bacillus pumilus LV149, an aquatic-derived probiotic, on gut injury repair in male C57BL/6 mice...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1507979/full |
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| author | Xinyu Sun Long Yun Keming Xie Renhui Liu Xinyue Ren Bokun Zeng Xudong Cao Zhi Li Guihao Zhou Bang Liu Luo Peng Lihong Yuan |
| author_facet | Xinyu Sun Long Yun Keming Xie Renhui Liu Xinyue Ren Bokun Zeng Xudong Cao Zhi Li Guihao Zhou Bang Liu Luo Peng Lihong Yuan |
| author_sort | Xinyu Sun |
| collection | DOAJ |
| description | PurposeGut microbiota dysbiosis significantly impacts ulcerative colitis (UC) progression and exacerbation. Probiotics show promise in UC management. This study evaluated the effects of different doses of Bacillus pumilus LV149, an aquatic-derived probiotic, on gut injury repair in male C57BL/6 mice with dextran sulfate sodium (DSS)-induced ulcerative colitis (UC) and investigated the underlying mechanisms.MethodsUC was induced by allowing mice free access to a 3% DSS solution for 7 days, with concurrent daily oral gavage of either a low (LV149-L, 1 × 108 CFU/day/mouse) or high (LV149-H, 1 × 109 CFU/day/mouse) dose of LV149. The effects were assessed through physiological parameters, intestinal barrier integrity, inflammation, gut microbiota composition, and transcriptomic changes.ResultsLV149 significantly improved pathological symptoms, including weight loss and disease activity index (DAI), and reduced colon shortening in a dose-dependent manner and inflammatory damage. The intervention also restored gut barrier function by upregulating mucins, goblet cell counts, and tight junction proteins (ZO-1, occludin, and claudin-1) in colonic tissue, along with reducing serum lipopolysaccharide (LPS) levels. Notably, only the LV149-H significantly decreased the expression of pro-inflammatory cytokines TNF-α, IL-1β, and IL-6, while both doses increased the expression of the anti-inflammatory cytokine IL-10 in a dose-dependent in colonic tissue. LV149 further modulated the gut microbiota, increasing beneficial bacteria and reducing pathogenic populations. Transcriptomic analysis indicated that LV149-L may exert gut repair effects via the IL-17 signaling pathway, whereas LV149-H appears to act through the JAK-STAT signaling pathway.ConclusionThis study demonstrated that LV149, particularly at a higher dose, effectively mitigated DSS-induced colonic injury by modulating gut microbiota, enhancing gut barrier integrity, and reducing inflammation. The dose-dependent effects underscored LV149-H’s potential as a therapeutic agent for UC due to its stronger anti-inflammatory properties and gut-protective effects. |
| format | Article |
| id | doaj-art-720453b4804a4072959baa8b0b1c7c03 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-720453b4804a4072959baa8b0b1c7c032025-01-08T15:51:47ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.15079791507979Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis miceXinyu Sun0Long Yun1Keming Xie2Renhui Liu3Xinyue Ren4Bokun Zeng5Xudong Cao6Zhi Li7Guihao Zhou8Bang Liu9Luo Peng10Lihong Yuan11School of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, ChinaHuzhou Key Laboratory of Translational Medicine, First Affiliated Hospital of Huzhou University, Huzhou, ChinaMedical College of Jiaying University, Jiaying University, Meizhou, ChinaSchool of Sports Medicine, Wuhan Sports University, Wuhan, ChinaSchool of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, ChinaSchool of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, ChinaDepartment of Chemical and Biological Engineering, University of Ottawa, Ottawa, ON, CanadaKey Laboratory of Aquacultural Biotechnology Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, ChinaDivision of Medicine, University College London, London, United KingdomSchool of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, ChinaKey Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, ChinaSchool of Life Sciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, ChinaPurposeGut microbiota dysbiosis significantly impacts ulcerative colitis (UC) progression and exacerbation. Probiotics show promise in UC management. This study evaluated the effects of different doses of Bacillus pumilus LV149, an aquatic-derived probiotic, on gut injury repair in male C57BL/6 mice with dextran sulfate sodium (DSS)-induced ulcerative colitis (UC) and investigated the underlying mechanisms.MethodsUC was induced by allowing mice free access to a 3% DSS solution for 7 days, with concurrent daily oral gavage of either a low (LV149-L, 1 × 108 CFU/day/mouse) or high (LV149-H, 1 × 109 CFU/day/mouse) dose of LV149. The effects were assessed through physiological parameters, intestinal barrier integrity, inflammation, gut microbiota composition, and transcriptomic changes.ResultsLV149 significantly improved pathological symptoms, including weight loss and disease activity index (DAI), and reduced colon shortening in a dose-dependent manner and inflammatory damage. The intervention also restored gut barrier function by upregulating mucins, goblet cell counts, and tight junction proteins (ZO-1, occludin, and claudin-1) in colonic tissue, along with reducing serum lipopolysaccharide (LPS) levels. Notably, only the LV149-H significantly decreased the expression of pro-inflammatory cytokines TNF-α, IL-1β, and IL-6, while both doses increased the expression of the anti-inflammatory cytokine IL-10 in a dose-dependent in colonic tissue. LV149 further modulated the gut microbiota, increasing beneficial bacteria and reducing pathogenic populations. Transcriptomic analysis indicated that LV149-L may exert gut repair effects via the IL-17 signaling pathway, whereas LV149-H appears to act through the JAK-STAT signaling pathway.ConclusionThis study demonstrated that LV149, particularly at a higher dose, effectively mitigated DSS-induced colonic injury by modulating gut microbiota, enhancing gut barrier integrity, and reducing inflammation. The dose-dependent effects underscored LV149-H’s potential as a therapeutic agent for UC due to its stronger anti-inflammatory properties and gut-protective effects.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1507979/fullBacillus pumilusulcerative colitisgut microbiotaintestinal mucosal barrierinflammationtranscriptomics |
| spellingShingle | Xinyu Sun Long Yun Keming Xie Renhui Liu Xinyue Ren Bokun Zeng Xudong Cao Zhi Li Guihao Zhou Bang Liu Luo Peng Lihong Yuan Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice Frontiers in Microbiology Bacillus pumilus ulcerative colitis gut microbiota intestinal mucosal barrier inflammation transcriptomics |
| title | Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice |
| title_full | Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice |
| title_fullStr | Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice |
| title_full_unstemmed | Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice |
| title_short | Probiotic Bacillus pumilus LV149 enhances gut repair, modulates microbiota, and alters transcriptome in DSS-induced colitis mice |
| title_sort | probiotic bacillus pumilus lv149 enhances gut repair modulates microbiota and alters transcriptome in dss induced colitis mice |
| topic | Bacillus pumilus ulcerative colitis gut microbiota intestinal mucosal barrier inflammation transcriptomics |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1507979/full |
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